Hybrids of Ixodes ricinus and Ixodes persulcatus ticks effectively acquire and transmit tick-borne encephalitis virus

Abstract

Ixodes rici nus and Ixodes persulcatus ticks are the main vectors of tick-borne encephalitis virus (TBEV), which has three main subtypes connected with certain tick species: the European subtype, associated with I. ricinus, and the Siberian and Far-Eastern subtypes, associated with I. persulcatus. Distribution ranges of these species overlap and form large sympatric areas in the East European Plain and Baltic countries. It has previously been shown that crossing of I. ricinus and I. persulcatus is possible, with the appearance of sterile hybrids. Hybridization of ticks can affect not only the spread of ticks but also the properties of natural foci of arbovirus infections, in particular TBEV. In the present study, we analyzed the effectiveness of virus transmission from infected mice to larvae and nymphs and trans-stadial transmission (from larvae to nymph and adult) in I. ricinus, I. persulcatus, and hybrids. For this purpose, we bred a hybrid generation from the crossing of I. persulcatus females and I. ricinus males, and we used the Siberian and European subtypes of TBEV. We showed that after feeding on infected mice, virus prevalence in engorged ticks decreased over time, and after molting, the opposite was true. In hybrids we observed the highest acquisition effectiveness and RNA copy numbers during Siberian TBEV subtype transmission. The efficiency of trans-stadial transmission of both TBEV subtypes was similar in hybrids and parental species. After the second trans-stadial TBEV transmission, a significant increase in ticks’ infection rates was observed only in specific subtype-tick combination. Our data demonstrate the possible features of TBEV circulation in the I. ricinus and I. persulcatus sympatry area.

Development Features of Ixodes ricinus × I. persulcatus Hybrids under Laboratory Conditions

“…To maintain the laboratory cultures, adult ticks were fed on rabbits ( Oryctolagus cuniculus (L., 1758), breed “Soviet Chinchilla”, “Scientific Center of Biomedical Technology” RAS, branch “Stolbovaya”) under a cloth cap, as described earlier [ 42 ]. Larvae and nymphs were fed on laboratory mice ( Mus musculus L., 1758, outbred ICR mice, “Scientific Center of Biomedical Technology” RAS, branch “Stolbovaya”), as described earlier [ 40 ]. All animals were maintained according to the international guidelines for animal husbandry, including the recommendations of CIOMS, 1985, and the FELASA Working Group Report, 1996–1997.…”

“…Experiments with mosquitoes showed that hybridization can impact vector competence [ 39 ], which in turn affects the risk of infection in natural foci. Recently, we were able to prove the competence of hybrids as TBEV vectors [ 40 ]. We showed that the hybrids from crossing I. persulcatus females with I. ricinus males were able to effectively acquire and transmit the TBEV of Siberian and European subtypes trans-stadially and to a susceptible host.…”

“…We showed that the hybrids from crossing I. persulcatus females with I. ricinus males were able to effectively acquire and transmit the TBEV of Siberian and European subtypes trans-stadially and to a susceptible host. Also, in hybrids, we observed the highest acquisition effectiveness and RNA copy numbers during Siberian TBEV subtype transmission [ 40 ]. To assess the local risk of infection with a tick-borne pathogen, it is necessary to have information about not only the tick infection rate and the properties of the pathogen but also about the seasonal course of activity and features of the life cycles of ticks.…”

Checklist of hosts, illustrated geographical range, and ecology of tick species from the genus Ixodes (Acari, Ixodidae) in Russia and other post-Soviet countries

“… pavlovskyi in Siberia with complete or partial coincidence of the seasonal activity of these species at each ontogenetic stage ( Ushakova and Filippova 1968 ; Bolotin et al 1977 ; Filippova 1999 ). In zones of sympatry their hybridization can occur, and their hybrids can also transmit tick-borne encephalitis virus and probably other pathogens ( Kovalev et al 2015 ; Rar et al 2019 ; Belova et al 2023 ). Under laboratory conditions, interspecific hybridization between I.…”

“… persulcatus , often exhibiting complete or partial coincidence of seasonal activity at each ontogenetic stage ( Filippova 1999 ). In zones of sympatry their hybridization can occur, and although hybrid offspring are incapable of reproduction ( Bugmyrin et al 2015 ), they can still transmit tick-borne encephalitis virus and probably other pathogens ( Kovalev et al 2016 ; Belova et al 2023 ). The absence of any morphological barrier for copulation was discovered in geographical points of probably the secondary sympatric zone ( Filippova 2002 ) of I.…”